Marine Ecology. ISSN 0173-9565
ORIGINAL ARTICLE
Relationships between mechanical disturbance and biomass
of the invasive amphipod Gammarus tigrinus within a
charophyte-dominated macrophyte community
Jonne Kotta1, Kaire Torn1, Greta Reisalu1 & Triin Veber1,2
1 Estonian Marine Institute, University of Tartu, Tallinn, Estonia
2 Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia
Keywords
Baltic Sea; Chara aspera; gammarid
amphipod; mechanical disturbance; nonnative species; recovery.
Correspondence
Jonne Kotta, Estonian Marine Institute,
University of Tartu, M€
aealuse 14, 12618
Tallinn, Estonia.
E-mail: jonne@sea.ee
Accepted: 13 December 2012
doi: 10.1111/maec.12073
Abstract
Disturbance may alter the resistance of communities to non-indigenous species
as it frees space and removes competitively superior species. In a factorial field
experiment we studied how different types of mechanical disturbance affected
the biomass level of the non-indigenous amphipod Gammarus tigrinus in a
brackish water charophyte community. Mechanical disturbance affected the
biomass of G. tigrinus with a time lag between disturbance and response of the
gammarid species. In general, all types of disturbance reduced gammarid biomasses. The effect persisted until the end of the experiment regardless of the
recovery of macrophyte communities in terms of species number and biomass
of benthic invertebrate and plant species. Thus, a possible cause of reduced
biomass of the gammarid amphipods relates to the decreased biomass of Chara
aspera and its structural changes. This indicates that the dominance of G. tigrinus in a low saline system has less to do with strong species interactions (e.g.
competitive displacement) than with habitat-level processes (e.g. changes in
habitat structural characteristics and food supply).
Introduction
Non-native species are ranked among the greatest threats
to global biodiversity (Bax et al. 2003), with coastal marine systems being the most invaded systems on the planet
(Carlton 1996). Earlier studies have shown that successful
exotics may render previously stable systems unbalanced
and unpredictable (Carlton 1996; Ruiz et al. 1997) and
severely affect the structure and functioning of invaded
ecosystems (Ricciardi & Cohen 2007; Orav-Kotta et al.
2009). Despite the importance of coastal invasions, marine non-native species are much less well studied than
terrestrial and freshwater counterparts (Grosholz 2002).
Dating back as far as 1958, Elton realized that speciesrich communities should be more stable and less susceptible to non-native species compared to species-poor
communities (Elton 1958). To date most of the smallerscale experimental work has supported this biotic resistance hypothesis (e.g. Stachowicz et al. 1999, 2002) and
Marine Ecology 35 (Suppl. 1) (2014) 11–18 ª 2013 Blackwell Verlag GmbH
the observed inverse relationship is explained by more
efficient utilization of available resources by highly diverse
communities (Levine & D’Antonio 1999) and/or the sampling effect, i.e., the occurrence of suppressive species
increases with diversity (Wardle 2001). Competition with
an ecologically similar native species is an obvious example of such biotic resistance (Kotta et al. 2001; Kotta &
Olafsson
2003).
Disturbance may alter the resistance of communities to
non-native species as it frees space and removes competitively superior species, thus relaxing competitive interactions among non-native and resident species (Shea &
Chesson 2002). Nevertheless, non-native species often
seem to have idiosyncratic and context-specific characters,
urging experimental studies on how disturbance affects
the population dynamics of these species. Even more, the
role of disturbance in the success of non-native species
has initiated a long debate because non-native species
could be considered the drivers or consequences of
11
Effects of mechanical disturbance on G. tigrinus biomass
biological changes (Didham et al. 2005 and references
therein).
Due to its short geological history, the Baltic Sea biota
has a low number of species (e.g. Segerstr
ale 1957).
Despite high numbers of non-native species, the coastal
biota shows no loss of biodiversity and, even more, nonnative species actually expand ecosystem functioning
(Kotta et al. 2006; Reise et al. 2006). In recent years the
range of non-native amphipods has increased tremendously in the Baltic Sea. Crustacean invaders seem to
expand their distribution at the expense of the resident
species of the area, suggesting strong competitive interactions among resident and non-native species (Jazdzewski
et al. 2002; Szaniawska et al. 2003; Orav-Kotta et al.
2009).
Although the exotic Gammarus tigrinus Sexton was
occasionally found in the southern Baltic Sea in the mid1970s, it was not until the early 2000s that the species
expanded its distribution throughout virtually the entire
Baltic (Herk€
ul et al. 2009). A recent climate change may
have facilitated this rapid range expansion, as elevated
winter storms are expected to increase the amount of
drifting macroalgae, an efficient transport vector of
amphipod crustaceans in the water column (Biber 2007).
More importantly, extensive erosion and alteration of
depositional coasts has been observed in the Baltic Sea in
recent years (Orviku et al. 2003). The lack of evidence for
sea level rise during this period suggests that such erosion
is largely due to the recent increased storminess in the
Eastern Baltic Sea. Severe storms efficiently erode sediment and destroy benthic macrophyte communities,
thereby facilitating the large-scale spread of the nonnative species through relaxation of competitive interactions. Besides these episodic extreme disturbances,
benthic communities are impoverished by increasing
intensities of smaller mechanical stressors, mainly of
human origin, such as trampling by feet, boating and
dredging.
Earlier studies have shown that G. tigrinus tolerates
broad environmental conditions (Pinkster et al. 1977;
Wijnhoven et al. 2003; Devin & Beisel 2007) and has low
habitat selectivity (Bousfield 1973; Daunys & Zettler
2006); therefore, it may potentially inhabit very different
types of coastal habitat. However, in the coastal reach of
the Northern Baltic Sea, the species is becoming a dominant mesoherbivore in the sheltered charophyte communities (Herk€
ul et al. 2009). Being extremely fragile, such
charophyte habitats are potentially very sensitive to any
type of mechanical disturbances.
In an in situ experiment, we studied how different
types of mechanical disturbance affected the biomass level
of G. tigrinus in a brackish water charophyte community.
We predict that a moderate mechanical disturbance leav12
Kotta, Torn, Reisalu & Veber
ing a significant proportion of the charophyte canopy
intact may increase the biomass of the non-native amphipod as the majority of native herbivores are expected to
be sensitive to such stress. Consequently, the competitive
interactions among non-native and resident species are
expected to be weakened (e.g. Herk€
ul et al. 2006).
Gammarus tigrinus is an opportunistic species and is
therefore expected to be less severely affected by mechanical disturbance than the resident species. We also predict
that due to the phytophilous nature of G. tigrinus, the
disturbances associated with mechanical removal of vegetation or sediment will significantly reduce the biomass
of the non-native species.
Study Area
Rame Bay is a shallow and semi-enclosed bay in the
Northeastern Baltic Sea (58.5749° N, 58.5671° E; surface
area 4 km2). The maximum depth of the area is 1.5 m
but most of the bay is shallower than 1 m. The bottom is
composed of fine sand and a thick layer of finely fractioned silt. Salinity varies between 3 and 5 and is highly
dependent on rainfall. Being sheltered, Rame Bay provides excellent habitat for luxurious charophyte populations together with aquatic phanerogams. The most
widespread species is Chara aspera Willd., which dominated the entire sheltered part of the bay (Torn & Martin
2003). The non-native amphipod Gammarus tigrinus only
recently invaded Rame Bay and 2 years after establishment (i.e., at the beginning of this study) it made up the
majority of gammarid abundance and biomass in the bay.
Material and Methods
Experimental procedures
The experiment was carried out from June 2007 to July
2008. Experimental plots (1.5 9 1.5 m) were established
within a dense Chara aspera community at 1 m depth.
Mechanical disturbance was applied once in June 2007
and involved the following treatment levels: (i) control
(i.e., undisturbed plots), (ii) cutting the tips of plants,
(iii) removal of plants, (iv) mixing of the sediment surface layer, (v) removal of the surface sediment layer. We
used a full random design. For the second treatment, the
upper 5 cm of the vegetation was cut by a diver. For the
third treatment, plants were removed gently by hand.
These two treatments mimic the foraging of herbivorous
birds. For the fourth treatment, sediment was mixed
together with vegetation to approximately 0.1 m depth.
Mixing of the sediment surface layer was used to imitate
the influence of motorboat anchoring, running of scooters and/or trampling. And finally, for the fifth treatment,
Marine Ecology 35 (Suppl. 1) (2014) 11–18 ª 2013 Blackwell Verlag GmbH
Effects of mechanical disturbance on G. tigrinus biomass
Kotta, Torn, Reisalu & Veber
the sediment layer was removed down to about 0.1 m
depth. Removal of the sediment layer represents disturbances due to dredging and/or ice scrape that also result
in the removal of vegetative layer. The plots were sampled
in July, August, September and October 2007, and July
2008. For each treatment level and sampling occasion
three replicate biomass samples were collected, totaling
75 samples. A SCUBA diver collected samples by gently
removing the biota within the algal canopy and sediment
epifauna using a 20 9 20 cm frame. Samples were stored
at 20 °C. In the laboratory all macrophytes and benthic
invertebrates were determined to the species level. The
dry weight of species was obtained after drying the individuals at 60 °C for 2 weeks (Torn et al. 2010).
Statistical analyses
Repeated measures ANOVA (StatSoft Inc 2007) was used
to compare the effect of different types of disturbance
(levels: tips cut, plants removed, sediment mixed, sediment
removed and control) on species number and biomass
among different months (from July 2007 to July 2008).
The Mauchly sphericity test was used to check the assumption of equality of variance. We used the following multivariate tests to seek the statistical significance of different
types of experimental disturbance on vegetation biomass:
Wilks’ lambda, Pillai–Bartlett trace and Hotelling–Lawley
trace tests. These tests were used as they do not make the
strict, often unrealistic, assumptions about the structure of
the covariance matrix. As all these tests resulted in similar
significance levels, only the output of the Wilks’ lambda
test (as the most commonly used) was reported. A posthoc Fisher LSD test was used to analyse which treatment
levels were statistically different from each other.
Multivariate data analyses on plant and invertebrate
communities were performed by the statistical program
PRIMER version 6.1.5 (Clarke & Gorley 2006). Similarities between each pair of samples were calculated using a
zero-adjusted Bray–Curtis coefficient. This coefficient is
known to outperform most other similarity measures and
enables samples containing no organisms at all to be
included (Clarke et al. 2006). Non-metric multidimensional scaling analysis (MDS) was used to visualize the
dissimilarities between treatments and times.
Results
The studied benthic invertebrate communities were characterized by a few taxa. The plots contained mainly the
amphipods Gammarus tigrinus, Gammarus salinus Spooner, Gammarus zaddachi Sexton, Gammarus oceanicus Segerstr
ale, Gammarus locusta (Linnaeus), the isopod Asellus
aquaticus (Linnaeus), the snails Bithynia tentaculata
Marine Ecology 35 (Suppl. 1) (2014) 11–18 ª 2013 Blackwell Verlag GmbH
(Linnaeus), Hydrobia ulvae (Pennant), Lymnaea peregra
(M€
uller), Theodoxus fluviatilis (Linnaeus), the cockle Cerastoderma glaucum (Poiret) and larvae of Chironomidae,
Coleoptera, Odonata and Trichoptera. Gammarus tigrinus
was by far the most dominant herbivore species and constituted 98% of gammarid biomass, with moderate biomasses
from June to September and high biomasses in October.
Mechanical disturbance affected the biomass of G. tigrinus with a 4-month time lag between disturbance and
response of the gammarid species (Fig. 1, Table 1).
Regardless of type, the disturbed communities had significantly lower gammarid biomasses than control communities in October 2007 (repeated measures ANOVA,
post-hoc Fisher LSD test: control versus disturbed plots
P < 0.001) and in July 2008 (repeated measures ANOVA,
post-hoc Fisher LSD test: control versus disturbed plots
P = 0.023–0.025, except for control versus tips cut treatment P = 0.071).
Mechanical disturbance had no effect on the species
number of benthic invertebrates and the biomasses of any
other invertebrate species including juvenile gammarids
(repeated measures ANOVA, separate disturbance effect
and disturbance 9 time interaction P > 0.05) (Fig. 2).
The studied macrophyte communities contained
mainly the charophyte Chara aspera, the chlorophytes
Cladophora glomerata (L.) K€
utz. and Ulva intestinalis L.
and the higher plants Najas marina L. and Potamogeton
Fig. 1. Seasonal variation in average (95%CI) biomass of
Gammarus tigrinus for the studied disturbance treatments in 2007–
2008.
Table 1. Repeated measures ANOVA multivariate test of significance
for the effect of disturbance on biomasses of Gammarus tigrinus in
2007–2008.
Effect
SS
Df
MS
F
P
Intercept
Disturbance
Error
TIME
TIME 9 disturbance
Error
35.70
16.44
2.94
16.92
20.06
10.99
1
4
10
4
16
40
35.70
4.11
0.29
4.23
1.25
0.27
121.35
13.98
<0.001
<0.001
15.40
4.56
<0.001
<0.001
13
Effects of mechanical disturbance on G. tigrinus biomass
Kotta, Torn, Reisalu & Veber
Fig. 3. Seasonal variation in average (95%CI) biomass of Chara
aspera for the studied disturbance treatments in 2007–2008.
Table 2. Repeated measures ANOVA multivariate test of significance
for the effect of disturbance on biomasses of Chara aspera in 2007–
2008.
Effect
SS
Df
MS
F
P
Intercept
Disturbance
Error
TIME
TIME 9 Disturbance
Error
311,731
258,034
1498
61,465
89,820
19,113
1
4
10
4
16
40
311,731
64,509
150
15,366
5614
478
2081
431
<0.001
<0.001
32
12
<0.001
<0.001
Fig. 2. Multidimensional scaling analysis (MDS) ordination of benthic
invertebrate and macrophyte biomasses. Increasing distances between
points denote larger dissimilarities among treatments and times. The
time code is as follows: 1: June 2007, 2: July 2007, 3: August 2007,
4: September 2007, 5: October 2007, 6: July 2008.
pectinatus L. Chara aspera was by far the most dominant
macrophyte species and constituted 96% of total plant
biomass, with high biomasses from June to September
and moderate biomasses in October.
Mechanical disturbance affected the biomass of
C. aspera instantaneously and the effects persisted until
the end of the experiment (Fig. 3, Table 2). Similarly to
G. tigrinus, the disturbed communities had significantly
lower biomasses compared with control communities. The
disturbances associated with mechanical removal of vegetation or sediment had the largest impact on the charophyte community throughout the experiment (repeated
measures ANOVA, post-hoc Fisher LSD test: control versus
heavily disturbed plots P < 0.001). Disturbances that only
partly damaged the plants had minor effects in 2007 and
the communities had recovered by July 2008.
Mechanical disturbance also reduced the species number of macrophytes (Fig. 4, Table 3). In general, the disturbances associated with mechanical removal of
vegetation or sediment had significantly lower species
number compared with other treatments in 2007
14
Fig. 4. Seasonal variation in average (95%CI) species number of
macrophytes for the studied disturbance treatments in 2007–2008.
Table 3. Repeated measures ANOVA multivariate test of significance
for the effect of disturbance on the species number of macrophytes
in 2007–2008.
Effect
SS
Df
MS
F
P
Intercept
Disturbance
Error
TIME
TIME 9 Disturbance
Error
730.080
35.387
4.933
27.653
37.547
16.400
1
4
10
4
16
40
730.080
8.847
0.493
6.913
2.347
0.410
1479.892
17.932
<0.001
<0.001
16.862
5.724
<0.001
<0.001
Marine Ecology 35 (Suppl. 1) (2014) 11–18 ª 2013 Blackwell Verlag GmbH
Kotta, Torn, Reisalu & Veber
(repeated measures ANOVA, post-hoc Fisher LSD test:
control versus heavily disturbed plots P < 0.05). Macrophyte species number within the heavily disturbed plots
had recovered by July 2008. Mechanical disturbance did
not affect the biomasses of other macrophyte species
(repeated measures ANOVA, separate disturbance effect
and disturbance 9 time interaction P > 0.05; Fig. 2).
Discussion
We predicted that a moderate mechanical disturbance that
leaves the charophyte community almost intact but at the
same time significantly impoverishes native invertebrate
communities, may increase the biomass of the non-native
amphipod because the competitive interactions are
relaxed. However, our experiment did not support this
prediction, as the biomass of Gammarus tigrinus was significantly reduced under all of the different types of
mechanical disturbance, whereas the native species were
not affected. The result suggests that the dominance of
G. tigrinus in our system has less to do with strong species
interactions, such as competitive displacement, than with
habitat-level processes, such as changes in habitat structural characteristics and food supply (e.g. Kotta et al.
2000, 2004, 2008b). Moreover, the experiment demonstrated that G. tigrinus constituted most of the benthic
invertebrate biomass. This would indicate that it is unlikely that G. tigrinus is influenced by competition from the
native fauna, as the native fauna is simply too sparse to
have significant competitive interactions with G. tigrinus.
Although there is solid evidence that disturbance
enhances the densities of non-native species both in terrestrial and aquatic ecosystems, the results are not fully
consistent. The effects of disturbance are known to be
scale-specific, with strong positive effects often associated
at small spatial scales but not at larger scales (Thompson
et al. 2001; Gross et al. 2005). At small spatial scales the
disturbance opens space in the community, which is then
quickly used by the opportunistic non-native and native
species and consequently animal densities at the community level are increased. On the other hand, disturbance
does not enhance the likelihood of a species to become
dominant, as high disturbance probably wipes out any
species including the opportunistic species. Such patterns
can be explained by purely statistical processes using neutral models with no species-specific interactions involved
(Herben 2009). However, the neutral model does not predict that the non-native species should prevail in the
absence of disturbance.
The Northeastern Baltic Sea is a physically limited
environment. Strong natural disturbances due to low
salinity, temperature extremes and ice scrape have
resulted in impoverished benthic communities, with
Marine Ecology 35 (Suppl. 1) (2014) 11–18 ª 2013 Blackwell Verlag GmbH
Effects of mechanical disturbance on G. tigrinus biomass
many native and alien species inhabiting the area at the
edge of their tolerance limits (Kotta et al. 2008a). In such
environments, competitive interactions are not expected
to play a large role; rather, habitat characteristics should
be responsible for shifts in the benthic communities. In
our experiment the strong link between the biomass of
Chara aspera and G. tigrinus suggests a strong affinity of
non-native gammarids to pristine charophyte habitats.
Nevertheless, none of the disturbance treatments had any
significant effect on the biomass of native species and
thus the expectation that the majority of native herbivores are sensitive to environmental stresses does not
hold true. We may also argue that the resistance of native
species is an inevitable consequence of natural selection,
as only the fittest can cope with the permanent environmental stresses presented by the Baltic Sea environment
(Herk€
ul et al. 2006).
Macrophytes provide important habitat and food
resources for a variety of associated mobile animals. This
is consistent with our study (and our second hypothesis)
in which dense charophyte communities supported high
biomasses of the non-native gammarid species. It is generally believed that mobile herbivores respond more strongly
to the amount of available resources than the diversity of
plants providing it (Parker et al. 2001; Christie et al.
2009), suggesting that mesoherbivores often have a broad
diet and selectivity is rare (Cruz-Rivera & Hay 2001). The
results of our experiment also hint that the gammarid
amphipods are generalist foragers, as high densities of
G. tigrinus did not match with macrophyte species number but rather to the biomass of C. aspera. It is plausible
that besides food value, dense charophyte communities
support high structural complexity and thus provide better value as a refuge from predators (Orav-Kotta & Kotta
2004; Kinzler & Mayer 2006; Christie et al. 2009).
Most aquatic macrophytes are seasonal, providing habitats of limited duration (Pihl et al. 1996; Kiirikki & Lehvo
1997), whereas species of gammarid amphipods have a
lifespan of approximately up to 3 years (e.g. Wilhelm &
Schindler 1996). Gammarids may therefore show a preference for macrophytes with higher longevity, such as
charophytes, over ephemeral algae. However, due to the
poor nutritional value of charophytes, grazers often just
live within their bushes and feed on the epiphytes attached
to the host plant (Coops & Doef 1996; Kotta et al. 2004).
The low levels of herbivory are also related to the unpalatability or resistance of the algae. According to Hunter
(1976), fresh Chara are heavily calcified, which may
greatly reduce their appeal to herbivores. In the course of
decomposition the cell walls of the algae become less resistant to herbivory and the concentration of nutrients
increases in the decomposing material as a result of
increased microbial activity (Hunter 1976; Buchsbaum
15
Effects of mechanical disturbance on G. tigrinus biomass
et al. 1991). As a consequence, the charophytes may occasionally become more attractive to benthic invertebrates,
especially in the late autumn months, when gammarids
are known to consume a significant number of charophytes (Van den Berg 1999; Noordhuis et al. 2002; Kotta
et al. 2004). By October, the density of filamentous algae
had notably declined in the study area. The abundant
population of G. tigrinus that had relied on these algae
was forced to switch to an alternative diet. Compared with
other macroalgae in the area, the decomposing charophytes seemed to be the most rewarding food for gammarid amphipods. Thus, high aggregation of G. tigrinus
within the Chara stands in October may be explained by
high mobility of G. tigrinus, ensuring high dispersal out of
macrophyte beds and quick utilization of rewarding habitats (e.g. Jørgensen & Christie 2003; Salovius et al. 2005).
Mechanical disturbance resulted in lower gammarid biomasses but such stress affected only the qualities of adult
habitats, whereas effects on juveniles were not found. The
statistical differences in the gammarid biomasses between
disturbed and undisturbed plots in October may be
explained partly as a statistical sampling effect, as it corresponds with the peak biomass of G. tigrinus.
However, G. tigrinus retained elevated biomasses within
undisturbed charophyte communities in July 2008, a year
after the disturbance. Although the communities of
C. aspera have recovered from moderate disturbances
(i.e., levels: tips cut, sediment mixed), G. tigrinus had a
systematically lower biomass in disturbed communities
than in control treatment and the biomasses did not vary
among disturbance levels. Thus, a high biomass of charophytes does not necessarily ensure that it will be colonized
by a high number of G. tigrinus. Instead, the availability
of resources and/or structural properties of charophytes
may better explain the recovery of gammarid amphipods
in the disturbed charophyte habitat. Repeated measures
ANOVA analysis showed that mechanical disturbance had
no effect on the algal resource availability, as assessed by a
ratio of the biomass of macroalgae to the biomass of G. tigrinus (repeated measures ANOVA, separate disturbance
effect and disturbance 9 time interaction P > 0.05). In
the light of this evidence, the lack of recovery of gammarid amphipods a year after the disturbance hints that the
three-dimensional structure of charophyte canopy rather
than absolute or relative algal quantity determines the
patterns of G. tigrinus in the studied habitat.
Conclusions
To conclude, mechanical disturbance affected the biomass
of Gammarus tigrinus but with a significant time lag,
possibly reflecting the seasonal dynamics of the gammarid
amphipods and macroalgae. In general, the disturbed
16
Kotta, Torn, Reisalu & Veber
communities had significantly lower gammarid biomasses
than control communities throughout the experiment.
A possible cause of reduced biomass of the gammarid
amphipods relates to the decreased biomass of C. aspera
and its structural changes but not to the diversity of macrophyte communities and the biomasses of macrophyte
and benthic invertebrate species. Thus, the dominance of
G. tigrinus in our system has less to do with strong species interactions, such as competitive displacement, than
with habitat-level processes, such as changes in habitat
structural characteristics and food supply.
Acknowledgements
Funding for this research was provided by by Institutional research funding IUT02-20 of the Estonian
Research Council and by the Estonian Science Foundation grants 7813 and 8254. The study has been partly
supported by the projects ‘EstKliima’ No. 3.2.0802.110043 and ‘The status of marine biodiversity and its
potential futures in the Estonian coastal sea’ No.
3.2.0801.11-0029 of the Environmental Protection and
Technology Programme of the European Regional Fund.
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